The Genomic Organization of Superorganismal Ant Colonies

From ancient philosophers like Aristotle to curious toddlers crawling in backyards, ants have long fascinated us. These tiny insects organize themselves into incredibly efficient colonies, with queens, workers, and sometimes even soldiers, each playing very distinct roles. But how could such highly sophisticated social coordination evolve?

Darwin’s Puzzle About Sterile Ant Workers and Highly Fertile Queens

In The Origin of Species (1859), Charles Darwin devoted quite a number of pages to ants, particularly to the workers who do not reproduce. He did not know about genes, but wondered how natural selection could have made queens and workers of the same colony so different even though they are closely related family members.

Darwin assumed that workers increase the reproductive success of their inseminated mother queen, thereby explaining the so-called reproductive division of labour: males provide sperm, which the queens store and use to fertilise eggs throughout their lives. Workers search for food, care for the brood and defend the nest, but do not mate and die young.

It has been known since the 1960s that Darwin was right: siblings can pass on gene copies to future generations just as effectively as own offspring can do. However, it was previously unclear how a complete restructuring of ant genomes took place so genomes could simultaneously contain genetic blueprints for the very different queens, males and workers in the same colony. A new international study with title Adaptive radiation and social evolution of the ants provides a large number of answers to this fundamental question.

Ant Genomes: Innovation, Stability and Diversification across 150 Million Years of Evolution

“We sequenced and compared high-quality genomes of more than 130 ant species from around the world, allowing us to resolve ant genomics to an unprecedented level of explanatory resolution”, says lead author Joel Vizueta.

Much of the structure of ant genomes can only be explained in relation to the emergence and subsequent modification of the queen and worker castes in colonies that are so tightly integrated that they are often referred to as superorganisms. The study covered ants with standard colony life, but also included fungus-farming ants, army ants with millions of workers per colony, ant species whose queens are a hundred times larger than the smallest workers, species without queens whose workers clone themselves, and social parasites that do not need any workers at all. “After the ants emerged more than 150 million years ago, natural selection consistently diversified their genomes into more than 15,000 currently known species representing a huge number of clever evolutionary innovations”, says Joel Vizueta.

Once the ancestral ant genome had become evolutionary stable in the early Cretaceous, its genes were recombined to an unusually high degree. This rearrangement was particularly extensive in the presently most species-rich ant subfamilies. At the same time, smaller groups of linked genes remained excluded from these rearrangements for more than 100 million years, especially those that mediate reproductive division of labour between queens and workers. “This unusual conservation of linked genes illustrates how fundamental the major evolutionary transition to differentiated caste societies was,” says Jacobus (Koos) Boomsma, the senior Copenhagen author of the study.

The GAGA Initiative Starts a New Era for Ant Genomics

The research leading to the new Cell paper was initiated in 2016 when Guojie Zhang, Jacobus Boomsma and Lukas Schrader started GAGA - the Global Ant Genomics Alliance, an initiative joined by more than 50 international researchers from more than 25 countries. “The results and data sets presented in our publication fundamentally innovate the study of social insect genomics”, Koos Boomsma concludes.